Sea spray allows for the growth of subaerial microbialites at the driest desert on Earth.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 08 2024
28 08 2024
Historique:
received:
18
04
2024
accepted:
16
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
28
8
2024
Statut:
epublish
Résumé
Due to its extreme conditions, microbial life in the Atacama Desert is known to survive in well-protected micro-habitats (hypolithic, endolithic, etc.), but rarely directly exposed to the environment, that is, epilithic habitats. Here we report a unique site, La Portada, a cliff confronting the Pacific Ocean in the Coastal Range of this desert, in which the constant input of water provided by the sea spray allows for the growth of a black-colored epilithic subaerial microbial ecosystem. Formed by a complex community of halophilic microorganisms belonging to the three domains of life, this ecosystem displays the typical three-dimensional structure of benthic microbialites, coherent with the presence of a diversity of cyanobacteria (including species from the genera that are known to form them), a constant high water activity and an ample availability of carbonate ions. From these microbialites we isolated Hortae werneckii, a fungal species which by producing melanin, not only explains the dark color of these microbialites, but may also play the role of protecting the whole community from extreme UV radiation. A number of biosignatures not only confirmed sea spray as the main source of water, but also suggests that one place to consider for the search of evidences of life on Mars would be on the paleo-coastlines that surrounded vanished oceans such as that on Aeolis Dorsa.
Identifiants
pubmed: 39198637
doi: 10.1038/s41598-024-70447-x
pii: 10.1038/s41598-024-70447-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
19915Subventions
Organisme : Human Frontiers Science Program
ID : RGY0066/2018
Organisme : Ministerio de Ciencia e Innovación
ID : PGC2021-124362NB-I00
Organisme : Spanish Ministry of Universities
ID : CA3/RSUE/2021-00405
Informations de copyright
© 2024. The Author(s).
Références
Encinas, A. et al. Tectonosedimentary evolution of the coastal Cordillera and central depression of South-Central Chile (36° 30′–42° S). Earth Sci. Rev. 213, 103465 (2021).
doi: 10.1016/j.earscirev.2020.103465
Cantalamessa, G. & Di Celma, C. Sedimentary features of tsunami backwash deposits in a shallow marine Miocene setting, Mejillones Peninsula, northern Chile. Sediment. Geol. 178, 259–273 (2005).
doi: 10.1016/j.sedgeo.2005.05.007
Hartley, A. J. et al. Palaeomagnetic evidence for rotation in the Precordillera of northern Chile: Structural constraints and implications for the evolution of the Andean forearc. Tectonophysics 205, 49–64 (1992).
doi: 10.1016/0040-1951(92)90417-5
Gérard, E. et al. Specific carbonate–microbe interactions in the modern microbialites of Lake Alchichica (Mexico). ISME J. 7, 1997–2009 (2013).
pubmed: 23804151
pmcid: 3965311
doi: 10.1038/ismej.2013.81
Burne, R. V. & Moore, L. S. Microbialites: Organosedimentary deposits of benthic microbial communities. Palaios 2, 241–254 (1987).
doi: 10.2307/3514674
Suarez-Gonzalez, P. et al. ‘Trapping and binding’: A review of the factors controlling the development of fossil agglutinated microbialites and their distribution in space and time. Earth Sci. Rev. 194, 182–215 (2019).
doi: 10.1016/j.earscirev.2019.05.007
Goguitchaichvili, A. T. et al. Paleomagnetism and rock-magnetism of the Jurassic La Negra Formation, Northern Chile: Implications for tectonics and volcanic stratigraphy. Int. Geol. Rev. 45, 563–573 (2003).
doi: 10.2747/0020-6814.45.6.563
Cordero, R. et al. Ultraviolet radiation in the Atacama Desert. Antonie van Leeuwenhoek 111, 1301–1313 (2018).
pubmed: 29605897
doi: 10.1007/s10482-018-1075-z
Williamson, A. et al. Complete genome sequence of Halomonas sp. R5–57. Stand Genom. Sci. 11, 62 (2016).
doi: 10.1186/s40793-016-0192-4
Zhang, H. et al. Salinimicrobium flavum sp. nov., isolated from coastal sediment. Int. J. Syst. Evol. Microbiol. 67, 4083–4088 (2017).
pubmed: 28901901
doi: 10.1099/ijsem.0.002257
Inoue, K. et al. Halomarina oriensis gen. nov., sp. nov., a halophilic archaeon isolated from a seawater aquarium. Int. J. Syst. Evol. Microbiol. 61, 942–946 (2011).
pubmed: 20495022
doi: 10.1099/ijs.0.020677-0
Cui, H. L. et al. Salinarchaeum laminariae gen. nov., sp. nov.: A new member of the family Halobacteriaceae isolated from salted brown alga Laminaria. Extremophiles 15, 625–631 (2011).
pubmed: 21901373
doi: 10.1007/s00792-011-0393-0
Takai, K. et al. Alkaliphilus transvaalensis gen. nov., sp. nov., an extremely alkaliphilic bacterium isolated from a deep South African gold mine. Int. J. Syst. Evol. Microbiol. 51, 1245–1256 (2001).
pubmed: 11491320
doi: 10.1099/00207713-51-4-1245
Yu, D. et al. Extremely halophilic denitrifying bacteria from hypersaline inland lakes, Halovibrio denitrificans sp. nov. and Halospina denitrificans gen. nov., sp. nov., and evidence that the genus name Halovibrio Fendrich 1989 with the type species Halovibrio variabilis should be associated with DSM 3050. Int. J. Syst. Evol. Microbiol. 56, 379–388 (2006).
doi: 10.1099/ijs.0.63964-0
Roh, S. W. et al. Haladaptatus cibarius sp. nov., an extremely halophilic archaeon from seafood, and emended description of the genus Haladaptatus. Int. J. Syst. Evol. Microbiol. 60, 1187–1190 (2010).
pubmed: 19667394
doi: 10.1099/ijs.0.013037-0
Denner, E. B. M. et al. Halococcus salifodinae sp. nov., an archaeal isolate from an Austrian salt mine. Int. J. Syst. Evol. Microbiol. 44, 774–780 (1994).
Zalar, P. et al. The extremely halotolerant black yeast Hortaea werneckii—A model for intraspecific hybridization in clonal fungi. IMA Fungus 10, 10 (2019).
pubmed: 32647617
pmcid: 7325687
doi: 10.1186/s43008-019-0007-5
Zajc, J. et al. Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl. Environ. Microb. 80, 247–256 (2014).
doi: 10.1128/AEM.02702-13
Ladas, N. P. & Papageorgiou, G. C. The salinity tolerance of freshwater cyanobacterium Synechococcus sp. PCC 7942 is determined by its ability for osmotic adjustment and presence of osmolyte sucrose. Photosynthetica 38, 343–348 (2000).
doi: 10.1023/A:1010957117237
Waditee-Sirisattha, R. et al. Global transcriptional and circadian regulation in a halotolerant cyanobacterium Halothece sp. PCC7418. Sci. Rep. 12, 13190 (2022).
pubmed: 35962002
pmcid: 9374696
doi: 10.1038/s41598-022-17406-6
Azua-Bustos, A. et al. Aeolian transport of viable microbial life on a Mars analog environment. Implications for Mars. Sci. Rep. 9, 1–11 (2019).
doi: 10.1038/s41598-019-47394-z
Zhu, T. & Dittrich, M. Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: A review. Front. Bioeng. Biotechnol. 20, 4 (2016).
Bosak, T. et al. Cyanobacterial diversity and activity in modern conical microbialites. Geobiology 10, 384–401 (2012).
pubmed: 22713108
doi: 10.1111/j.1472-4669.2012.00334.x
Schneider, D. et al. Phylogenetic analysis of a microbialite-forming microbial mat from a hypersaline lake of the kiritimati atoll, central pacific. PLoS ONE 8, e66662 (2013).
pubmed: 23762495
pmcid: 3677903
doi: 10.1371/journal.pone.0066662
Nguyen, S. T. et al. Bacterial community structure and metabolic potential in microbialite-forming mats from South Australian saline lakes. Geobiology 20, 546–559 (2022).
pubmed: 35312212
pmcid: 9311741
doi: 10.1111/gbi.12489
Lamérand, C. et al. Carbon sequestration potential of Mg carbonate and silicate biomineralization in the presence of cyanobacterium Synechococcus. Chem. Geol. 599, 120854 (2022).
doi: 10.1016/j.chemgeo.2022.120854
Sorokovikova, E. et al. Limnofasciculus baicalensis gen. et sp. nov. (Coleofasciculaceae, Coleofasciculales): A new genus of cyanobacteria isolated from sponge fouling in Lake Baikal, Russia. Microorganisms 11, 1779 (2023).
pubmed: 37512951
pmcid: 10385159
doi: 10.3390/microorganisms11071779
Verrecchia, E. P. et al. Spherulites in calcrete laminar crusts: Biogenic CaCO3, precipitation as a major contributor to crust formation. J. Sediment. Res. A65, 690–700 (1995).
Read, J. F. Calcretes and their distinction from stromatolites. Dev. Sedimentol. 20, 55–71 (1976).
doi: 10.1016/S0070-4571(08)71129-4
Wu, Y. et al. Cyanobacterial fossils from 252 Ma old microbialites and their environmental significance. Sci. Rep. 4, 3820 (2014).
pubmed: 24448025
pmcid: 3898040
doi: 10.1038/srep03820
Lagier, J. C. et al. Genome sequence of Oceanobacillus picturae strain S1, an halophilic bacterium first isolated in human gut. Stand. Genom. Sci. 10, 91 (2015).
doi: 10.1186/s40793-015-0081-2
Shin, N. R. et al. Ornithinibacillus scapharcae sp. nov., isolated from a dead ark clam. Antonie Van Leeuwenhoek 101, 147–154 (2012).
pubmed: 21952732
doi: 10.1007/s10482-011-9645-3
Dehvari, M. et al. Petroleum contaminated seawater detoxification in microcosm by halotolerant consortium isolated from Persian Gulf. Curr. Microbiol. 78, 95–106 (2021).
pubmed: 33159563
doi: 10.1007/s00284-020-02267-x
Hu, Y. J. et al. Research progress on salt tolerance and growth-promoting mechanism of Bacillus. Biotechnol. Bull. 36, 64 (2020).
Mtibaà, R. A halotolerant laccase from Chaetomium strain isolated from desert soil and its ability for dye decolourization. 3Biotech 7, 329 (2017).
Picazo, I. et al. Defining the transcriptional responses of Aspergillus nidulans to cation/alkaline pH stress and the role of the transcription factor SltA. Microb. Genom. 6, 000415 (2020).
Paul, S. I. et al. Identification of marine sponge-associated bacteria of the Saint Martin’s island of the Bay of Bengal emphasizing on the prevention of motile Aeromonas septicemia in Labeo rohita. Aquaculture 545, 737156 (2021).
doi: 10.1016/j.aquaculture.2021.737156
Sáez-Nieto, J. A. et al. Paenibacillus spp. isolated from human and environmental samples in Spain: Detection of 11 new species. New Microbes New Infect. 19, 19–27 (2017).
pubmed: 28702198
pmcid: 5484988
doi: 10.1016/j.nmni.2017.05.006
Kamat, S. et al. Endophytic fungus, Chaetomium globosum, associated with marine green alga, a new source of Chrysin. Sci. Rep. 10, 18726 (2020).
pubmed: 33127928
pmcid: 7603332
doi: 10.1038/s41598-020-72497-3
Xing, C. et al. Steroids and anthraquinones from the deep-sea-derived fungus Aspergillus nidulans MCCC 3-A. Biochem. Syst. Ecol. 83, 103–105 (2019).
doi: 10.1016/j.bse.2018.12.012
Azua-Bustos, A. et al. A novel subaerial Dunaliella sp. Growing on cave spiderwebs in the Atacama Desert. Extremophiles 14, 443–452 (2010).
pubmed: 20623153
doi: 10.1007/s00792-010-0322-7
Vondrak, J. & Kubásek, J. Algal stacks and fungal stacks as adaptations to high light in lichens. The Lichenologist 45, 115–124 (2013).
doi: 10.1017/S0024282912000722
Azua-Bustos, A. et al. Dark microbiome and extremely low organics in Atacama fossil delta unveil Mars life detection limits. Nat. Commun. 14, 808 (2023).
pubmed: 36810853
pmcid: 9944251
doi: 10.1038/s41467-023-36172-1
Finkel, P. L. et al. An overview of lipid biomarkers in terrestrial extreme environments with relevance for mars exploration. Astrobiology 23, 563–604 (2023).
pubmed: 36880883
pmcid: 10150655
doi: 10.1089/ast.2022.0083
Kaneda, T. Iso- and anteiso-fatty acids in bacteria: Biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55, 288–302 (1991).
pubmed: 1886522
pmcid: 372815
doi: 10.1128/mr.55.2.288-302.1991
van den Brink, D. M. et al. Phytanic acid: Production from phytol, its breakdown and role in human disease. Cell Mol. Life Sci. 63, 1752–1765 (1966).
doi: 10.1007/s00018-005-5463-y
Roca-Saavedra, P. et al. Phytanic acid consumption and human health, risks, benefits and future trends: A review. Food Chem. 15, 237–247 (2017).
doi: 10.1016/j.foodchem.2016.10.074
Didyk, B. M. et al. Organic geochemical indicators of palaeoenvironmental conditions of sedimentation. Nature 272, 216–222 (1978).
doi: 10.1038/272216a0
Stalport, F. et al. Investigating the photostability of carboxylic acids exposed to mars surface ultraviolet radiation conditions. Astrobiology 9, 543–549 (2009).
pubmed: 19663761
doi: 10.1089/ast.2008.0300
Pacelli, C. Fungal biomarkers are detectable in Martian rock-analogues after space exposure: Implications for the search of life on Mars. Int. J. Astrobiol. 20, 1–14 (2021).
doi: 10.1017/S1473550421000240
Korablev, O. I. Infrared spectrometer for ExoMars: A mast-mounted instrument for the rover. Astrobiology 17, 542–564 (2017).
pubmed: 28731817
doi: 10.1089/ast.2016.1543
Cardenas, B. T. & Lamb, M. P. Paleogeographic reconstructions of an ocean margin on Mars based on deltaic sedimentology at Aeolis Dorsa. J. Geophys. Res. Planets 127, e2022JE007390 (2022).
doi: 10.1029/2022JE007390
Grimalt, J. O. et al. Sedimentary lipid biogeochemistry of an hypereutrophic alkaline lagoon. Geochim. Cosmochim. Acta 55, 2555–2577 (1991).
doi: 10.1016/0016-7037(91)90373-D
Sánchez-García, L. et al. Molecular biomarkers in the subsurface of the Salar Grande (Atacama, Chile) evaporitic deposits. Biogeochemistry 140, 31–52 (2018).
doi: 10.1007/s10533-018-0477-3
Schelbe, R. T. et al. Community structure comparison using FAME analysis of desert varnish and soil, Mojave Desert, California. Geomicrobiol. J. 22, 353–360 (2005).
doi: 10.1080/01490450500248754
Culka, A. et al. Raman microspectrometric study of pigments in melanized fungi from the hyperarid Atacama Desert gypsum crust. J. Raman Spectrosc. 48, 1487–1493 (2017).
doi: 10.1002/jrs.5137